Models of toxic β-sheet channels of protegrin-1 suggest a common subunit organization motif shared with toxic Alzheimer β-amyloid ion channels

Biophysical Journal

Volumn 95, Issue 10, 2008, Pages 4631-4642

  Jang, Hyunbum ^a   Ma, Buyong ^a   Lal, Ratnesh ^b   Nussinov, Ruth ^a,c  

^a SAIC FREDERICK INC   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; ANTIMICROBIAL CATIONIC PEPTIDE; ION CHANNEL; PROTEGRIN 1; PROTEGRIN-1; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; PROTEIN CONFORMATION; PROTEIN MOTIF; ULTRASTRUCTURE;

AMINO ACID MOTIFS; AMYLOID BETA-PROTEIN; ANTIMICROBIAL CATIONIC PEPTIDES; COMPUTER SIMULATION; ION CHANNELS; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN SUBUNITS;

EID: 58149311146     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.134551     Document Type: Article

References (48)

1. Sitaram, N., and R. Nagaraj. 2002. Host-defense antimicrobial peptides: importance of structure for activity. Curr. Pharm. Des. 8:727-742.
2. Hancock, R. E., and A. Rozek. 2002. Role of membranes in the activities of antimicrobial cationic peptides. FEMS Microbiol. Lett. 206:143-149.
3. Kourie, J. I., and A. A. Shorthouse. 2000. Properties of cytotoxic peptide-formed ion channels. Am. J. Physiol. Cell Physiol. 278:C1063-C1087.
4. Zasloff, M. 2002. Antimicrobial peptides of multicellular organisms. Nature. 415:389-395.
5. Sokolov, Y., T. Mirzabekov, D. W. Martin, R. I. Lehrer, and B. L. Kagan. 1999. Membrane channel formation by antimicrobial protegrins. Biochim. Biophys. Acta. 1420:23-29.
6. Yang, L., T. M. Weiss, R. I. Lehrer, and H. W. Huang. 2000. Crystallization of antimicrobial pores in membranes: magainin and protegrin. Biophys. J. 79:2002-2009.
7. Brogden, K. A. 2005. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3:238-250.
8. Fahrner, R. L., T. Dieckmann, S. S. Harwig, R. I. Lehrer, D. Eisenberg, and J. Feigon. 1996. Solution structure of protegrin-1, a broad-spectrum antimicrobial peptide from porcine leukocytes. Chem. Biol. 3:543-550.
9. Kokryakov, V. N., S. S. Harwig, E. A. Panyutich, A. A. Shevchenko, G. M. Aleshina, O. V. Shamova, H. A. Korneva, and R. I. Lehrer. 1993. Protegrins: leukocyte antimicrobial peptides that combine features of corticostatic defensins and tachyplesins. FEBS Lett. 327:231-236.
10. Miyasaki, K. T., and R. I. Lehrer. 1998. Beta-sheet antibiotic peptides as potential dental therapeutics. Int. J. Antimicrob. Agents. 9:269-280.
11. Mani, R., S. D. Cady, M. Tang, A. J. Waring, R. I. Lehrer, and M. Hong. 2006. Membrane-dependent oligomeric structure and pore formation of a beta-hairpin antimicrobial peptide in lipid bilayers from solid-state NMR. Proc. Natl. Acad. Sci. USA. 103:16242-16247.
12. Tang, M., A. J. Waring, and M. Hong. 2007. Phosphate-mediated arginine insertion into lipid membranes and pore formation by a cationic membrane peptide from solid-state NMR. J. Am. Chem. Soc. 129:11438-11446.
13. Buffy, J. J., A. J. Waring, and M. Hong. 2005. Determination of peptide oligomerization in lipid bilayers using 19F spin diffusion NMR. J. Am. Chem. Soc. 127:4477-4483.
14. Tang, M., A. J. Waring, and M. Hong. 2005. Intermolecular packing and alignment in an ordered β-hairpin antimicrobial peptide aggregate from 2D solid-state NMR. J. Am. Chem. Soc. 127:13919-13927.
15. Mani, R., M. Tang, X. Wu, J. J. Buffy, A. J. Waring, M. A. Sherman, and M. Hong. 2006. Membrane-bound dimer structure of a beta-hairpin antimicrobial peptide from rotational-echo double-resonance solid-state NMR. Biochemistry. 45:8341-8349.
16. Herce, H. D., and A. E. Garcia. 2007. Molecular dynamics simulations suggest a mechanism for translocation of the HIV-1 TAT peptide across lipid membranes. Proc. Natl. Acad. Sci. USA. 104:20805-20810.
17. Mecke, A., D. K. Lee, A. Ramamoorthy, B. G. Orr, and M. M. Banaszak Holl. 2005. Membrane thinning due to antimicrobial peptide binding: an atomic force microscopy study of MSI-78 in lipid bilayers. Biophys. J. 89:4043-4050.
18. Chen, F. Y., M. T. Lee, and H. W. Huang. 2003. Evidence for membrane thinning effect as the mechanism for peptide-induced pore formation. Biophys. J. 84:3751-3758.
19. Heller, W. T., A. J. Waring, R. I. Lehrer, T. A. Harroun, T. M. Weiss, L. Yang, and H. W. Huang. 2000. Membrane thinning effect of the beta-sheet antimicrobial protegrin. Biochemistry. 39:139-145.
20. Jang, H., B. Ma, T. B. Woolf, and R. Nussinov. 2006. Interaction of protegrin-1 with lipid bilayers: membrane thinning effect. Biophys. J. 91:2848-2859.
21. Jang, H., B. Ma, and R. Nussinov. 2007. Conformational study of the protegrin-1 (PG-1) dimer interaction with lipid bilayers and its effect. BMC Struct. Biol. 7:21.
22. Gidalevitz, D., Y. Ishitsuka, A. S. Muresan, O. Konovalov, A. J. Waring, R. I. Lehrer, and K. Y. Lee. 2003. Interaction of antimicrobial peptide protegrin with biomembranes. Proc. Natl. Acad. Sci. USA. 100:6302-6307.
23. Sitaram, N., and R. Nagaraj. 1999. Interaction of antimicrobial peptides with biological and model membranes: structural and charge requirements for activity. Biochim. Biophys. Acta. 1462:29-54.
24. Hancock, R. E., and R. Lehrer. 1998. Cationic peptides: a new source of antibiotics. Trends Biotechnol. 16:82-88.
25. Ludtke, S. J., K. He, Y. Wu, and H. W. Huang. 1994. Cooperative membrane insertion of magainin correlated with its cytolytic activity. Biochim. Biophys. Acta. 1190:181-184.
26. Quist, A., I. Doudevski, H. Lin, R. Azimova, D. Ng, B. Frangione, B. Kagan, J. Ghiso, and R. Lal. 2005. Amyloid ion channels: a common structural link for protein-misfolding disease. Proc. Natl. Acad. Sci. USA. 102:10427-10432.
27. Lin, H., R. Bhatia, and R. Lal. 2001. Amyloid beta protein forms ion channels: implications for Alzheimer's disease pathophysiology. FASEB J. 15:2433-2444.
28. Lau, T. L., E. E. Ambroggio, D. J. Tew, R. Cappai, C. L. Masters, G. D. Fidelio, K. J. Barnham, and F. Separovic. 2006. Amyloid-beta peptide disruption of lipid membranes and the effect of metal ions. J. Mol. Biol. 356:759-770.
29. Lashuel, H. A., D. Hartley, B. M. Petre, T. Walz, and P. T. Lansbury Jr. 2002. Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature. 418:291.
30. Kawahara, M., and Y. Kuroda. 2000. Molecular mechanism of neurodegeneration induced by Alzheimer's beta-amyloid protein: channel formation and disruption of calcium homeostasis. Brain Res. Bull. 53:389-397.
31. Arispe, N., H. B. Pollard, and E. Rojas. 1994. beta-Amyloid Ca(2+)-channel hypothesis for neuronal death in Alzheimer disease. Mol. Cell. Biochem. 140:119-125.
32. Jang, H., J. Zheng, R. Lal, and R. Nussinov. 2008. New structures help the modeling of toxic amyloidbeta ion channels. Trends Biochem. Sci. 33:91-100.
33. Jang, H., J. Zheng, and R. Nussinov. 2007. Models of beta-amyloid ion channels in the membrane suggest that channel formation in the bilayer is a dynamic process. Biophys. J. 93:1938-1949.
34. Hirakura, Y., and B. L. Kagan. 2001. Pore formation by beta-2-microglobulin: a mechanism for the pathogenesis of dialysis associated amyloidosis. Amyloid. 8:94-100.
35. Hirakura, Y., R. Azimov, R. Azimova, and B. L. Kagan. 2000. Polyglutamine-induced ion channels: a possible mechanism for the neurotoxicity of Huntington and other CAG repeat diseases. J. Neurosci. Res. 60:490-494.
36. Lin, M. C., T. Mirzabekov, and B. L. Kagan. 1997. Channel formation by a neurotoxic prion protein fragment. J. Biol. Chem. 272:44-47.
37. Castano, S., B. Desbat, and J. Dufourcq. 2000. Ideally amphipathic beta-sheeted peptides at interfaces: structure, orientation, affinities for lipids and hemolytic activity of (KL)(m)K peptides. Biochim. Biophys. Acta. 1463:65-80.
38. Bechinger, B. 2000. Understanding peptide interactions with the lipid bilayer: a guide to membrane protein engineering. Curr. Opin. Chem. Biol. 4:639-644.
39. Zakharov, S. D., E. A. Kotova, Y. N. Antonenko, and W. A. Cramer. 2004. On the role of lipid in colicin pore formation. Biochim. Biophys. Acta. 1666:239-249.
40. Allende, D., S. A. Simon, and T. J. McIntosh. 2005. Melittin-induced bilayer leakage depends on lipid material properties: evidence for toroidal pores. Biophys. J. 88:1828-1837.
41. Jang, H., N. Michaud-Agrawal, J. M. Johnston, and T. B. Woolf. 2008. How to lose a kink and gain a helix: pH independent conformational changes of the fusion domains from influenza hemagglutinin in heterogeneous lipid bilayers. Proteins. 72:299-312.
42. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM - a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4:187-217.
43. Smart, O. S., J. M. Goodfellow, and B. A. Wallace. 1993. The pore dimensions of gramicidin A. Biophys. J. 65:2455-2460.
44. Phillips, J. C., R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R. D. Skeel, L. Kale, and K. Schulten. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:1781-1802.
45. Allen, T. W., O. S. Andersen, and B. Roux. 2006. Molecular dynamics - potential of mean force calculations as a tool for understanding ion permeation and selectivity in narrow channels. Biophys. Chem. 124:251-267.
46. de Groot, B. L., and H. Grubmuller. 2001. Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science. 294:2353-2357.
47. Leontiadou, H., A. E. Mark, and S. J. Marrink. 2007. Ion transport across transmembrane pores. Biophys. J. 92:4209-4215.
48. Roumestand, C., V. Louis, A. Aumelas, G. Grassy, B. Calas, and A. Chavanieu. 1998. Oligomerization of protegrin-1 in the presence of DPC micelles. A proton high-resolution NMR study. FEBS Lett. 421:263-267.